A network of multiple regulatory layers shapes gene expression in fission yeast

被引:162
作者
Lackner, Daniel H.
Beilharz, Traude H.
Marguerat, Samuel
Mata, Juan
Watt, Stephen
Schubert, Falk
Preiss, Thomas
Bahler, Juerg [1 ]
机构
[1] Wellcome Trust Sanger Inst, Canc Res UK, Fiss Yeast Funct Genom Grp, Cambridge CB10 1HH, England
[2] Victor Chang Cardiac Res Inst, Mol Genet Program, Darlinghurst, NSW 2010, Australia
[3] Univ New S Wales, St Vincents Clin Sch, Sydney, NSW 2052, Australia
[4] Univ New S Wales, Sch Biotechnol & Biomol Sci, Sydney, NSW 2052, Australia
基金
英国惠康基金;
关键词
GENOME-WIDE ANALYSIS; POSTTRANSCRIPTIONAL CONTROL; EUKARYOTIC TRANSLATION; REVEALS WIDESPREAD; MESSENGER-RNAS; CODON USAGE; INITIATION; TRANSCRIPTOME; MICROARRAYS; DROSOPHILA;
D O I
10.1016/j.molcel.2007.03.002
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Gene expression is controlled at multiple layers, and cells may integrate different regulatory steps for coherent production of proper protein levels. We applied various microarray-based approaches to determine key gene-expression intermediates in exponentially growing fission yeast, providing genome-wide data for translational profiles, mRNA steady-state levels, polyadenylation profiles, start-codon sequence context, mRNA half-lives, and RNA polymerase 11 occupancy. We uncovered widespread and unexpected relationships between distinct aspects of gene expression. Translation and polyadenylation are aligned on a global scale with both the lengths and levels of mRNAs: efficiently translated mRNAs; have longer poly(A) tails and are shorter, more stable, and more efficiently transcribed on average. Transcription and translation may be independently but congruently optimized to streamline protein production. These rich data sets, all acquired under a standardized condition, reveal a substantial coordination between regulatory layers and provide a basis for a systems-level understanding of multilayered gene-expression programs.
引用
收藏
页码:145 / 155
页数:11
相关论文
共 49 条
[1]   Dissecting eukaryotic translation and its control by ribosome density mapping [J].
Arava, Y ;
Boas, FE ;
Brown, PO ;
Herschlag, D .
NUCLEIC ACIDS RESEARCH, 2005, 33 (08) :2421-2432
[2]   Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae [J].
Arava, Y ;
Wang, YL ;
Storey, JD ;
Liu, CL ;
Brown, PO ;
Herschlag, D .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2003, 100 (07) :3889-3894
[3]   Gene Ontology annotation status of the fission yeast genome: preliminary coverage approaches 100% [J].
Aslett, Martin ;
Wood, Valerie .
YEAST, 2006, 23 (13) :913-919
[4]   Autoregulation of ribosome biosynthesis by a translational response in fission yeast [J].
Bachand, F ;
Lackner, DH ;
Bähler, J ;
Silver, PA .
MOLECULAR AND CELLULAR BIOLOGY, 2006, 26 (05) :1731-1742
[5]  
Beilharz Traude H., 2004, Briefings in Functional Genomics & Proteomics, V3, P103, DOI 10.1093/bfgp/3.2.103
[6]   Post-transcriptional expression regulation in the yeast Saccharomyces cerevisiae on a genomic scale [J].
Beyer, A ;
Hollunder, J ;
Nasheuer, HP ;
Wilhelm, T .
MOLECULAR & CELLULAR PROTEOMICS, 2004, 3 (11) :1083-1092
[7]   Global transcriptional responses of fission yeast to environmental stress [J].
Chen, DR ;
Toone, WM ;
Mata, J ;
Lyne, R ;
Burns, G ;
Kivinen, K ;
Brazma, A ;
Jones, N ;
Bähler, J .
MOLECULAR BIOLOGY OF THE CELL, 2003, 14 (01) :214-229
[8]   Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, Arabidopsis [J].
Duret, L ;
Mouchiroud, D .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1999, 96 (08) :4482-4487
[9]   Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast [J].
Gerber, AP ;
Herschlag, D ;
Brown, PO .
PLOS BIOLOGY, 2004, 2 (03) :342-354
[10]   Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors [J].
Grigull, J ;
Mnaimneh, S ;
Pootoolal, J ;
Robinson, MD ;
Hughes, TR .
MOLECULAR AND CELLULAR BIOLOGY, 2004, 24 (12) :5534-5547